The photic‐aphotic divide is a strong ecological and evolutionary force determining the distribution of ciliates (Alveolata, Ciliophora) in the ocean

Abstract

The bulk of knowledge on marine ciliates is from shallow and/or sunlit waters. We studied ciliate diversity and distribution across epi‐ and mesopelagic oceanic waters, using DNA metabarcoding and phylogeny‐based metrics. We analyzed sequences of the 18S rRNA gene (V4 region) from 369 samples collected at 12 depths (0–1000 m) at the Bermuda Atlantic Time‐series Study site of the Sargasso Sea (North Atlantic) monthly for 3 years. The comprehensive depth and temporal resolutions analyzed led to three main findings. First, there was a gradual but significant decrease in alpha‐diversity (based on Faith's phylogenetic diversity index) from surface to 1000‐m waters. Second, multivariate analyses of beta‐diversity (based on UniFrac distances) indicate that ciliate assemblages change significantly from photic to aphotic waters, with a switch from Oligotrichea to Oligohymenophorea prevalence. Third, phylogenetic placement of sequence variants and clade‐level correlations (EPA‐ng and GAPPA algorithms) show Oligotrichea, Litostomatea, Prostomatea, and Phyllopharyngea as anti‐correlated with depth, while Oligohymenophorea (especially Apostomatia) have a direct relationship with depth. Two enigmatic environmental clades include either prevalent variants widely distributed in aphotic layers (the Oligohymenophorea OLIGO5) or subclades differentially distributed in photic versus aphotic waters (the Discotrichidae NASSO1). These results settle contradictory relationships between ciliate alpha‐diversity and depth reported before, suggest functional changes in ciliate assemblages from photic to aphotic waters (with the prevalence of algivory and mixotrophy vs. omnivory and parasitism, respectively), and indicate that contemporary taxon distributions in the vertical profile have been strongly influenced by evolutionary processes. Integration of DNA sequences with organismal data (microscopy, functional experiments) and development of databases that link these sources of information remain as major tasks to better understand ciliate diversity, ecological roles, and evolution in the ocean.

Role of Syndiniales parasites in depth-specific networks and carbon flux in the oligotrophic ocean

“…For example, Syndiniales composition varied by season (PERMANOVA R 2 = 0.2 and 0.11; P -value < 0.001) at depths in the photic zone (e.g., 1 and 120 m), while seasonal changes were not significant at deeper depths (e.g., 600 and 1000 m). Other 18S rRNA gene metabarcoding studies at this site [ 33 , 34 ] and in the North Pacific [ 17 ] have noted significant variability in protist composition and diversity with depth compared with weaker seasonal signals. Seasonality in the Sargasso Sea is characterized by deep convective mixing (~150–300 m) between January and March and stratification of the water column (mixed layer depth < 20 m) as early as May [ 32 ], driving seasonal patterns in phytoplankton, heterotrophic bacteria, and viruses [ 39–41 ].…”

“…Recent 18S rRNA gene metabarcoding work at BATS revealed a high relative abundance of Syndiniales (~40%) throughout the water column [ 33 ] and their presence in sediment traps [ 20 ]. Moreover, several studies at BATS [ 33 , 34 ], and in other oligotrophic systems [ 17 ], have observed significant shifts in protist diversity and composition with depth, with communities varying less over seasonal cycles. We performed covariance network analysis of a 4-year (2016–19) 18S rRNA gene metabarcoding dataset [ 33 ], constructing networks for each of 12 discrete depths (1–1000 m).…”

Diversity and distribution of small-sized planktonic ciliate communities in the East China Sea

“…Surface water in the ECS is mainly mixed by the CDW, KSW, and TCWW, while the deeper layer is influenced by KSSW, Shelf Mixing Water (SMW), and TCWW by the Optimum Multiparameter analysis (Zhou et al, 2018). Ciliate community composition and diversity reported differ markedly with depth (Countway et al, 2010;Grattepanche et al, 2016a, b;Santoferrara et al, 2023;Tucker et al, 2017;Zhao et al, 2017;Wang et al, 2021a), water masses (Sun et al, 2020;Yang et al, 2020;Gu et al, 2021), and geographical position (inshore/offshore) (Grattepanche et al, 2015;Santoferrara et al, 2016;Grattepanche et al, 2016b). While Yang et al (2020) indicated that planktonic ciliates were potentially reliable indicators of water masses in the ECS, this was not universally consistent, possibly due to methodological differences in definitions of water masses or ciliate analysis approaches (Zhang et al, 2015).…”